Download Regional biogeography of shallow reef fish and macro

Journal of Biogeography (J. Biogeogr.) (2004) 31, 1107–1124
ORIGINAL
ARTICLE
Regional biogeography of shallow reef
fish and macro-invertebrate communities
in the Galapagos archipelago
G. J. Edgar*, S. Banks, J. M. Fariña , M. Calvopiña and C. Martı́nez
Charles Darwin Research Station, Santa Cruz,
Galapagos, Ecuador
ABSTRACT
Aim To delineate biogeographical patterns in Galapagos shallow-water reef
fauna at regional scales.
Location Galapagos Islands.
Methods Fishes and macro-invertebrates were quantitatively censused using
underwater visual techniques along more than 500 transects at defined depth
strata across the Galapagos archipelago. Data were analysed using multivariate
techniques to define regional patterns and identify species typical of different
regions.
Results Subtidal communities of fishes and macro-invertebrates on shallow
reefs differed consistently in species composition across the Galapagos
archipelago, with three major biogeographical groupings: (1) the ‘far-northern
area’ containing the islands of Darwin and Wolf, (2) the ‘central/south-eastern
area’, including the east coast of Isabela, and (3) the ‘western area’, encompassing
Fernandina and western Isabela. In addition, the northern islands of Pinta,
Marchena and Genovesa form a separate region in the central/south-eastern area,
and Bahia Elizabeth and Canal Bolivar separate from other parts of the western
area. The far-northern bioregion is characterized by high fish species richness
overall, including a high proportion of species of Indo-Pacific origin. However,
very few endemic fishes or species with distributions extending south from
Ecuador (‘Peruvian’ species) are present, and the bioregion also possesses
relatively low species richness of mobile macro-invertebrate taxa. By contrast, the
‘western’ bioregion possesses disproportionately high numbers of endemic fish
taxa, high numbers of cool-temperate Peruvian fish species, and high invertebrate
species richness, but very few species of Indo-Pacific origin. The Bahia Elizabeth/
Canal Bolivar bioregion possesses more endemic species and fewer species with
Peruvian affinities than coasts within the western bioregion. The northern
bioregion of Pinta, Marchena and Genovesa represents an overlap zone with
affinities to both the far-northern and south-eastern islands. The south-eastern
bioregion includes species from a variety of different sources, particularly
‘Panamic’ species with distributions extending north to Central America.
*Correspondence: G. J. Edgar, School of
Zoology, Tasmanian Aquaculture and Fisheries
Institute, University of Tasmania, GPO Box 25205, Hobart, Tasmania 7001, Australia.
E-mail: [email protected]
Present address: J. M. Fariña, Center for
Advanced Studies in Ecology and Biodiversity
(CASEB), Pontificia Universidad Católica de
Chile, Santiago, Chile and Department of
Ecology and Evolutionary Biology, Brown
University, Providence, RI 02912, USA.
Main conclusions On the basis of congruent divisions for reef fish and macroinvertebrate communities, the Galapagos archipelago can be separated into three
major biogeographical areas, two of which can be further subdivided into two
regions. Each of these five bioregions possesses communities characterized by a
distinctive mix of species derived from Indo-Pacific, Panamic, Peruvian and
endemic source areas. The conservation significance of different regions is not
reflected in counts of total species richness. The regions with the lowest overall
fish species richness possess a temperate rather than tropical climate and highest
levels of endemism.
ª 2004 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi
1107
G. J. Edgar et al.
Keywords
Benthos, Galapagos, fishes, macro-invertebrates, reef, biogeographical region,
species richness, endemism, faunal distribution.
INTRODUCTION
The more than 100 volcanic islands and islets of Galapagos
possess one of the most interesting biogeographical settings on
earth. Galapagos is the only tropical archipelago lying at the
intersection of major warm- and cool-water current systems,
being located in the path of (1) the warm south-westerly
flowing Panama Current, (2) the cool north-westerly flowing
Peru current, and (3) the cold eastward-flowing subsurface
equatorial undercurrent (Houvenaghel, 1978; Banks, 2002).
The latter rises to the surface along western and southern
margins of the Galapagos Plateau, generating highly productive upwelling systems (Pak & Zanfield, 1974). As a
consequence, oceanographical conditions vary markedly over
short spatial scales across the archipelago, with quite extreme
environmental differences existing between the cool upwelling
region in the west and the warm oligotrophic north. For
example, water temperature at 10 m depth at Punta Espinosa
on the westernmost island of Fernandina averaged 18 C
compared with 24 C 180 km north off the island of Wolf
between June 1996 and February 1997 (Wellington et al.,
2001). Much of this regional variation in ocean climate
disappears during El Niño years (Banks, 2002), when water
temperatures rise above 25 C throughout the archipelago for
periods that can exceed a year (Wellington et al., 2001).
The anomalous ocean climate surrounding Galapagos
translates to distinctive marine ecosystems that occur in close
proximity, and a biota that includes elements characteristic of
tropical (e.g. manta rays, reef sharks, corals), temperate (sea
lions, kelp) and even subantarctic (fur seals, penguins,
albatross) seas. A large component of endemic species is
present (Bustamante et al., 2000), notably including the marine
iguana (Amblyrhynchus cristatus), flightless cormorant (Phalacrocorax harrisi) and the only tropical laminarian kelp (Eisenia
galapagensis).
Despite this scientific importance, little has been published
on the distribution of marine biodiversity across the region
(Bensted-Smith, 2002). The most widely quoted marine
regionalization for the archipelago was described more than
30 years ago by Harris (1969). This regionalization was
originally physical rather than biological, with water temperature data used as a surrogate for biological data because the
latter were largely lacking (Harris, 1969). In the Harris scheme,
Galapagos waters were subdivided into five regions (north,
west, south, central and central mixing). Jennings et al. (1994)
provided some support for Harris’ (1969) scheme with
information on reef fishes; however, only 10 sites were
investigated during that study and insufficient data were
available to compare variation within as well as between
regions. In the sole major archipelago-wide investigation prior
1108
to the present study, Wellington (1975) considered that four
major biogeographical regions were clearly defined for Galapagos (western, southern, central and northern).
The present study aimed to clarify broad-scale marine
biogeographical patterns across Galapagos. It was initiated
partly for scientific interest and partly in response to a
management need. All waters extending 40 miles offshore from
an imaginary line joining the outer islands are regulated by the
Ecuadorian Government for conservation of biodiversity
within the Galapagos Marine Reserve (GMR). The GMR is
regulated by a Management Plan, which states as a principal
aim that biodiversity will be protected in all biogeographical
regions. The Management Plan was negotiated by local
stakeholders, who recognized that marine plants and animals
required protection within ‘no-take’ sanctuary zones of
adequate size in all different bioregions. This aim could only
be achieved if biogeographical regions were more accurately
defined than currently in the Harris scheme.
METHODS
Sites surveyed
Quantitative data were collected between 13 May 2000 and
13 December 2001 during research cruises to define baseline
conditions in different management zones within the GMR.
The shallow subtidal rocky reef habitat investigated here, and
used as the data set for deriving the regionalization, represents
the predominant habitat type around the Galapagos coastline
(> 95% of shallow habitat, Bustamante et al., 2002). Shallow
reefs also comprise the habitat most affected by fishing and
other human activity.
Underwater visual censuses along line transects were undertaken during daylight hours at 50 islands and islets distributed
across the archipelago (Fig. 1). Generally, two different depth
contours were surveyed at a single site. For some sites, the two
depth strata surveyed were parallel and immediately adjacent to
each other, while in other areas depth strata were offset by up to
300 m when divers were working from different boats.
Consequently, the term ‘site’ is somewhat ambiguous, and
the term ‘depth strata’ preferred, referring to one depth interval
at a site. Overall, a total of 579 and 569 depth strata were
surveyed for fish and macro-invertebrates, respectively.
Faunal survey protocols
Fish surveys were undertaken by laying a 50 m transect line
along a defined depth contour within the range from 2 to 20 m
depth. A diver swam beside the transect line at a distance of
2.5 m, recording on a waterproof notepad the abundance of
Journal of Biogeography 31, 1107–1124, ª 2004 Blackwell Publishing Ltd
fishes in a 5 m wide swathe (i.e. from the transect line out to a
distance of 5 m). This process was then repeated on return
along the other side of the transect line, with data from the two
adjoining sides of the transect added together for each
50 m · 10 m census block. For the majority (59%) of depth
strata, two replicate 50 m · 10 m blocks were surveyed and
mean data for that depth stratum used in analyses; however, on
the remaining occasions the census block was not duplicated.
Macro-invertebrates were censused along the same transect
lines as for fishes. However, only a 1 m wide swathe up and
back along the transect line was surveyed by the diver, who
recorded the abundance of macro-invertebrate species (sea
stars, sea cucumbers, sea urchins, octopus, large gastropods,
large bivalves, spiny lobsters and large crabs) in each
2 m · 50 m block. As with analyses of fishes, the majority of
depth strata were duplicated, and the mean value for the two
blocks used in analyses.
Analyses
The number of species recorded during 50 m transects at
depth strata across the archipelago was plotted in Arcview
(ESRI, Redlands, CA, USA). Smoothed contour plots were
produced using the Inverse Distance Weighted interpolation
function with 24 nearest neighbours along the coastline.
Offshore extrapolations have been masked in figures using a
10 km corridor off the coast.
Faunal relationships between sites were investigated using
non-metric multidimensional scaling (MDS) plots calculated
by PRIMER (Plymouth, UK; Carr, 1996). These provided the
best graphical depictions in two dimensions of biological
similarities between sites.
Because data for individual transects were greatly affected by
local environmental conditions, particularly depth and wave
exposure, and the aim of the study was to identify regional
patterns, site data were grouped by calculating a mean value
for each 10 depth strata in nearest proximity around the coast
of each island. Data matrices showing mean abundances of
different fish or invertebrate species at different sites used for
MDS plots were initially fourth root-transformed, then
converted to matrices of biotic similarity between pairs of
sites using the Bray–Curtis similarity index, as recommended
by Faith et al. (1987). The usefulness of the two-dimensional
MDS display of biotic relationships is indicated by the stress
statistic, which signifies a good depiction of relationships when
< 0.1 and poor depiction when > 0.2 (Clarke, 1993).
Additionally, the SIMPER module of PRIMER was used to
identify species that contributed most substantially to the
average similarity within each biogeographical region, and
thereby typified each region (Clarke, 1993).
Analysis of the macro-invertebrate data set (Fig. 4) reveals
three major groups of sites: (1) Darwin and Wolf, (2)
Fernandina and western Isabela, and (3) other islands.
Genovesa and Pinta also separate from the main island
grouping because of their greater affinity with the fauna of
Darwin and Wolf. The fauna of Marchena is quite variable but
with a high level of similarity to central and southern islands
and north-eastern Isabela. The fauna of Pinzon is distinctive.
The macro-invertebrate fauna also shows a very high degree
of variation around Isabela, but is more homogeneous around
Fernandina than was seen for the fish fauna (Fig. 5). The
invertebrate fauna off the coast of Isabela from Punta
Albermarle to Cuatro Hermanos overlaps the fauna of
Floreana, Santiago, Santa Fe, Santa Cruz, San Cristobal,
Espanola and Rabida, while the west coast fauna exhibits
major differences between Bahia Elizabeth (Islas Marielas) and
Caleta Iguana.
Patterns of fish species richness (i.e. the number of fish
species observed per 50 m · 10 m transect block) across the
archipelago generally reflected clinal trends in communities
identified by MDS. Fish species richness was highest around
the far-northern islands of Darwin and Wolf and lowest off
Fernandina, Santa Cruz, and the Bahia Elizabeth region of
western Isabela (Fig. 6). However, the distribution of endemic
Galapagos fishes was opposite to that seen for the total fauna,
with endemic species present in highest numbers near Islas
Marielas in Bahia Elizabeth and also off western Isabela,
Fernandina, Santa Fé and south-western Floreana (Fig. 7).
The unusually high species richness in the far-northern
region was caused by the presence in that area of numerous
species with ranges extending westward across the Indo-Pacific
(Fig. 8a). Many of these species were coral reef-associated
wrasses, butterflyfishes, pufferfishes and jacks. The far-northern islands also possessed a disproportionately high number
of species with ‘Panamic’ ranges that extend north of Ecuador
but not south (Fig. 8b); nevertheless, in addition to the virtual
absence of endemic Galapagos fishes (Fig. 7), this region
included very few species with ‘Peruvian’ ranges extending
south along the South American coast (Fig. 8d).
Southward-ranging Peruvian species were largely restricted
to western, northern and southern Fernandina, and southwestern and north-western Isabela (Fig. 8d), probably because
most of these species associate with seaweed habitats that are
largely absent elsewhere in the archipelago. Fish species with
wide South American ranges that extended both north and
south of Ecuador were widespread throughout the archipelago
(Fig. 8c), except for disproportionately low numbers off Bahia
Elizabeth, Fernandina (particularly the east coast) and Santa
Cruz.
In contrast to the situation with fishes, the number of
macro-invertebrate species recorded per 50 m · 2 m transect
block varied relatively little across the archipelago, with a
general average of 6.0 species per transect (Fig. 9). Nevertheless, 25% fewer species occurred around the far-northern
islands of Darwin and Wolf (4.5 species per transect) than
elsewhere.
Invertebrate species with Indo-Pacific distributions occurred
throughout the archipelago, with lowest species richness in the
south-west (Fig. 10a). Species with ranges only to the north of
Ecuador were also widely distributed but with no decline
apparent in the western region (Fig. 10b). The relatively low
species richness of macro-invertebrates around the two
northernmost islands was caused by few species with widespread South American distributions occurring in the farnorthern area (Fig. 10c). Widespread South American
species were, however, disproportionately abundant off western
Isabela and Fernandina, and presumably tolerated cooler
conditions than the other regional species groups.
No macro-invertebrate species were sighted that possessed a
distribution on the South American continent solely south
G. J. Edgar et al.
92°
91°
90°
89°
2°
2°
Management zones
Conservation
Tourism
Fishing
Port
1°
1°
Species
0°
0°
1°
1°
92°
91°
90°
89°
92°
91°
90°
89°
10
11
12
13
14
15
16
17
18
19
20
21
22
23
Figure 6 Shaded contour plot showing
mean total number of fish species observed
per 50 m transect around different coasts of
Galapagos. Line width of island outline
reflects management zone of that section of
coast.
2° Management zones
2°
Conservation
Tourism
Fishing
Port
1°
1°
Species
0°
0°
1°
1°
92°
91°
90°
Figure 7 Shaded contour plot showing
mean total number of endemic Galapagos
fish species per 50 m transect.
89°
from Ecuador. Moreover, only four endemic invertebrate
species were recorded in transects – the slipper lobster
Scyllarides astori, the sea urchin Eucidaris galapagensis, the
octopus Octopus oculifer and the scallop Nodipecten magnificus,
hence plots of macro-invertebrates comparable with Figs 7 and
8d could not be depicted.
Generally, species richness analyses for fish and invertebrate
data sets were consistent with MDS analyses in showing that
Galapagos coastal waters are best divided into the five marine
biogeographical regions (bioregions) shown in Fig. 11. These
bioregions are referred to as ‘far-northern’, ‘northern’, southeastern’, ‘western’ and ‘Elizabeth’. The name ‘Elizabeth’ has
1112
0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
been used because the core features of that bioregion are most
evident within Bahia Elizabeth rather than Canal Bolivar,
which possess more overlap with the ‘western’ bioregion. The
Elizabeth bioregion extends from Punta Espinosa and the
northern point of Tagus Cove in the north to Punta Mangle
and just east of Punta Moreno in the south. The western
bioregion on Isabela extends from just west of Punta
Albermarle to just east of Isla Tortuga.
The mean densities of common fish and invertebrate species
in different bioregions are listed in Tables 1 and 2. Species
disproportionately abundant or rare in each bioregion, as
identified using SIMPER analysis (Clarke, 1993), are also
Journal of Biogeography 31, 1107–1124, ª 2004 Blackwell Publishing Ltd
Regional biogeography of Galapagos shallow-water reef fauna
92°
91°
90°
89°
92°
91°
90°
89°
2°
2° 2°
2°
1°
1° 1°
1°
0°
0° 0°
0°
1°
1° 1°
1°
(a)
(b)
92°
92°
91°
91°
90°
90°
92°
92°
89°
89°
91°
91°
90°
90°
89°
89°
2°
2°
1°
1°
0°
0°
1°
1°
(c)
(d)
92°
91°
90°
92°
89°
91°
90°
89°
Figure 8 Shaded contour plot showing mean total number of fish species per 50 m transect for species with Panamic (ranges extending
northwards along the South American coast but not southwards from Ecuador), Indo-Pacific (ranges extending westwards to at least
Hawaii), Peruvian (ranges extending southwards along the South American coast but not northwards from Ecuador) and widespread
(ranges extending both northwards and southwards along the South American coast from Ecuador) ranges.
indicated. Note that species showing disproportionately high
mean abundances within a bioregion are not necessarily
identified by SIMPER analysis as typifying that bioregion. For
example, the endemic goby Lythrypnus gilberti is most
abundant in the south-eastern bioregion but better typifies
the Elizabeth bioregion. This fish occurred in extremely high
abundance (> 1 m)2) at a few sites on south-western Isabela in
the south-eastern bioregion but was absent from the majority
of sites, whereas the species occurred in lower maximal
abundance in the Elizabeth bioregion but at a high proportion
of sites.
Faunal abundance data for different biogeographical regions
exhibited similar patterns to species richness data in that
densities of Indo-Pacific species were generally highest in the
far-northern bioregion, endemic species were most abundant
in the Elizabeth and western bioregions, and Peruvian species
were most abundant in the western bioregion. Nevertheless, a
few anomalous distributions existed. For example, the IndoPacific pufferfish Sphoeroides annulatus was not recorded in
the far-northern islands while the parrotfish Scarus ghobban
was widely distributed throughout the archipelago rather than
being concentrated in the far north. In addition, although the
echinoid Echinometra vanbrunti and the holothurian Holothuria difficilis possess Panamic distributions, these species were
not detected in the warm far-northern region of Galapagos.
Faunal data pertaining to different 0.01 latitude and
longitude grid cells have been classified in multidimensional
space using CAP analysis to maximize differences between the
five bioregional groups. The best congruence with the five
bioregional groups was found using the first 20 principal
Journal of Biogeography 31, 1107–1124, ª 2004 Blackwell Publishing Ltd
1113
components for fishes and first 10 principal components for
macro-invertebrates. Differences between bioregional groups
were statistically significant for all pairwise comparisons
(permutation test, P < 0.001, including Bonferoni correction
for 10 pairwise tests).
For both fishes (Fig. 12) and macro-invertebrates (Fig. 13),
the first two canonical axes did not separate the western and
Elizabeth regions (Figs 12a and 13a); hence the third canonical
axes have been included in figures (Figs 12b and 13b).
Although these figures indicate a stronger separation between
the western and Elizabeth bioregions for fishes than invertebrates, the leave-one-out procedure indicates a stronger
separation between these bioregions for the macro-invertebrate
data when all canonical axes are considered (Tables 3 and 4).
Data for each grid cell were accurately classified into the
appropriate bioregional group in the majority of cases using
the leave-one-out procedure, with misclassification primarily
occurring between the western and Elizabeth bioregions, and
between the northern and south-eastern bioregions. Thus, a
primary three-group separation exists between far-northern,
northern + south-eastern, and western + Elizabeth bioregions.
Species showing high correlations with the major canonical
axes included nearly all species identified by SIMPER analysis
as typifying particular regions. A large group of species,
including the moray eel Gymnothorax dovii, surgeonfishes
Acanthurus nigricans and Prionurus laticlavius, priacanthid
Heteropriacanthus cruentatus, trumpetfish Aulostomus chinensis, Moorish idol Zanclus cornutus, pufferfishes Arothron
meleagris and Canthigaster punctatissima, wrasse Thalassoma
lucasanum, triggerfish Sufflamen verres, sea urchin Diadema
mexicanum, spiny lobster Panulirus penicillatus and crab
Percnon gibbesi, were principally confined to the far-northern
islands. The majority of these species possess Indo-Pacific
distributions.
The groupers Paralabrax albomaculatus and Mycteroperca
olfax, goby Lythrypnus gilberti, sea cucumber Stichopus fuscus,
and sea stars Nidorellia armata and Pharia pyramidata were
most highly correlated with the Elizabeth bioregion; the wrasse
Halichoeres dispilus, weedfish Labrisomus dendriticus, and sea
urchins Lytechinus semituberculatus and Centrostephanus coronatus with the western bioregion; and the wrasses Semicossyphus darwini and Bodianus eclancheri, hornshark Heterodontus
quoyi, and knifejaw Oplegnathus insignis were disproportionately abundant in both these bioregions. Species highly
correlated with the south-eastern region included the damselfish Abudefduf troschelii, wrasse Halichoeres nicholsi, grunt
Haemulon scudderi, and sea urchin Tripneustes depressus. The
holothurians Holothuria atra and Holothuria fuscocinerea were
primarily associated with the northern bioregion.
DISCUSSION
Biogeographical patterns
Faunal abundance and species richness data both indicate that
Galapagos inshore reef ecosystemshoi09.shore78406.7visiblhore
te Lyeehat
differing from the fish fauna of Santa Cruz and possessing
relatively close affinity to the northern islands (Fig. 2) – these
patterns were not consistent for both the fish and macroinvertebrate data sets. Furthermore, the variation around
individual islands was considerable (as seen, e.g. in Fig. 4 for
invertebrates around Santa Cruz) and often greater than
variation between islands. Hence, using our fish and invertebrate data sets, we were unable to subdivide the various central,
eastern and southern islands into consistent subgroups.
The distinctiveness of the Elizabeth grouping was an
unexpected outcome of the analysis. In terms of faunistic
affinity, the core of the Elizabeth bioregion around Islas
Marielas differed from Caleta Iguana as much as Caleta Iguana
did from south-eastern islands such as Santa Cruz. Part of the
reason for this distinctiveness can be inferred from satellite
images of the GMR depicting phytoplankton concentration
(Banks, 2002); nearly all images indicate much higher levels of
primary productivity in the Elizabeth bioregion than elsewhere
in the archipelago. This high productivity may give the
ecosystem its distinctive character.
The strong regional divisions in the Galapagos marine
fauna probably reflect both local environmental conditions
and connectivity of larval propagules with external source
regions. Species with Indo-Pacific distributions occur predominantly in the far-northern region of Galapagos, where
water temperatures are highest, turbidity is low, coral
development is most extensive, and warm currents are likely
to first strike the archipelago. Many amongst the diverse farnorthern component of species probably maintain gene flow
across the East Pacific Barrier, particularly during El Niño
years when currents from the north-east and north prevail
(Glynn & Ault, 2000). In addition to long-lasting larval
stages, Indo-Pacific fishes in Galapagos often penetrate much
more widely through the archipelago during periods of El
Niño, and possess small local population sizes and distorted
size structures (Grove, 1985). Some species (most notably the
wrasse Stethojulis bandanensis) apparently recruit to the
archipelago episodically only during El Niño years (Victor
et al., 2001).
Populations of Panamic species are probably largely selfsustaining in Galapagos but with intermittent recruitment
from the mainland and islands to the north. Amongst the local
fish species of Panamic origin where the duration of larval
stage has been examined, some individuals have been found to
settle onto reefs after periods insufficient for long-distance
transport, whereas others possess long larval stages and
predominantly recruit during El Niño years (Wellington &
Victor, 1992; Meekan et al., 2001).
The Peruvian component of species is probably largely selfsustaining within Galapagos rather than reliant on larval
propagules arriving from the continent. Populations of Peruvian species primarily occur in western rather than southeastern Galapagos – the geographically closer location to the
southern South American coast. Peruvian species presumably
prefer the west because environmental conditions are colder
with high primary production, and thus more similar to
prevailing environmental conditions in central South America.
All of the endemic species encountered during surveys are
closely related to species present on the South American coast
(see e.g. Lessios et al., 1999).
Patterns of species richness across the archipelago were
dissimilar for fishes and macro-invertebrate, in part because
macro-invertebrate species with Peruvian affinities were
absent and endemic invertebrate species were depauperate.
Representation of these groups within the Galapagos fauna
has probably declined greatly during recent decades, particularly following the 1982/83 El Niño. This is indicated, for
example, by a collapse in populations of the endemic scallop
Nodipecten magnificus, a large mollusc that occurred commonly in the Elizabeth bioregion until 1983. In that year, all
living individuals monitored by researchers died (Robinson,
1985). Scallop numbers have shown little subsequent recovery, with only three individuals recorded during recent
surveys. Several other endemic invertebrate species, including
the corals Tubastraea floreana Wells and Madrepora galapagensis Vaughan and the seastar Heliaster solaris (A.H. Clark),
have not been sighted since 1983 (Cairns, 1991; Hickman,
1998).
The 1982/83 El Niño clearly had a catastrophic impact on
Galapagos marine biodiversity, with consequences that persist
today (Bensted-Smith, 2002). Macroalgae and invertebrates
with cool-temperate affinities appear to have been most
affected (also corals: Glynn, 1994), their ranges contracting
greatly and populations now being largely confined to localized
areas in the west. Thus, patterns of invertebrate biodiversity
identified would perhaps have been quite different if our
surveys had been conducted in 1980.
The poor recovery of marine invertebrates following El Niño
compared with fishes is likely due to limited metapopulation
Regional biogeography of Galapagos shallow-water reef fauna
Table 1 Mean abundance per 500 m2 transect in different biogeographical regions of fish species recorded on at least five transects.
Fish species identified using SIMPER analysis to be associated with particular bioregions are listed by superscript in rank order of strength of
association, with negative numbers indicating negative association
Biogeographical region
Species
Endemic species
Lythrypnus gilberti (Heller & Snodgrass)
Xenocys jessiae Jordan & Bollman
Girella freminvillei (Valenciennes)
Orthopristis forbesi Jordan & Starks
Lepidonectes corallicola (Kendall & Radcliffe)
Acanthemblemaria castroi Stephens & Hobson
Mugil rammelsbergi (Ebeling)
Paralabrax albomaculatus (Jenyns)
Sphoeroides angusticeps (Jenyns)
Odontoscion eurymesops (Heller & Snodgrass)
Panamic species
Thalassoma lucasanum (Gill)
Prionurus laticlavius Valenciennes
Stegastes beebei (Nichols)
Apogon atradorsatus Heller & Snodgrass
Stegastes arcifrons (Heller & Snodgrass)
Microspathodon dorsalis (Gill)
Johnrandallia nigrirostris (Gill)
Haemulon scudderi Gill
Mycteroperca olfax (Jenyns)
Lutjanus viridis (Valenciennes)
Halichoeres nicholsi (Jordan & Gilbert)
Labrisomus dendriticus (Reid)
Cirrhitus rivulatus Valenciennes
Chromis alta Greenfield & Woods
Lutjanus aratus (Günther)
Scarus compressus (Osborn & Nichols)
Microspathodon bairdii (Gill)
Thalassoma grammaticum Gilbert
Kyphosus elegans (Peters)
Cephalopholis panamensis (Steindachner)
Dermatolepis dermatolepis (Boulenger)
Canthigaster punctatissima (Günther)
Gymnothorax dovii (Günther)
Sargocentron suborbitalis (Gill)
Euthynnus lineatus Kishinouye
Myripristis leiognathos Valenciennes
Lutjanus novemfasciatus(Gill)
Dasyatis brevis (Garman)
Coryphopterus urospilus Ginsburg
Synodus lacertinus Gilbert
Scorpaena mystes Jordan & Starks
Hypsoblennius brevipinnis (Günther)
Hoplopagrus guentheri Gill
Peruvian species
Anisotremus scapularis (Tschudi)
Bodianus eclancheri (Valenciennes)
Sphyraena idiastes Heller & Snodgrass
Oplegnathus insignis (Kner)
Semicossyphus darwini (Jenyns)
Heterodontus quoyi (Freminville)
Far-northern
0
0
0.02
0
0.16
0
0
0
0
0
1027.9
123.2
21.6)2
0.08
13.9
0.91
7.41
0
0.06
0.33
0.07
0.60
1.41
0.19
0
0.18
0.95
1.95
1.50
0.36
1.65
0.74
1.90
0.05
0
0.03
0.17
0
0
0.17
0.15
0
0.07
0.12
0
0
0.10
0
0
Northern
0
0.63
0.60
0.10
0.26
0
0.10
0.46
0.10
0
158.8
141.5
76.5
0.08
22.5
6.61
7.93
0
1.74
1.96
0.69
1.22
1.96
0.43
0.63
1.31
0.58
0.20
0.44
0.41
0.25
0.71
0.82
0.25
1.06
0.39
0.18
0.02
0.02
0.01
0.04
0
0.01
0.02
0
0
0
0
0
Journal of Biogeography 31, 1107–1124, ª 2004 Blackwell Publishing Ltd
South-eastern
24.6
6.87
2.64
4.38
1.47
2.20
0.39
0.15
0.10
0
Western
Elizabeth
Overall
1.40
41.0
2.57
1.62
4.45
1.56
0
0.09
0.02
0.35
17.62
20.3
2.01
1.88
2.514
0.01
8.06
1.345
0.07
0
15.2
12.1
2.09
2.80
1.77
1.41
1.06
0.30
0.08
0.05
123.2
118.6
81.8
24.3
8.30
6.43
6.03
6.00
3.92
3.56
2.56
2.55
1.77
1.49
1.08
0.96
0.94
0.59
0.36
0.32
0.30
0.28
0.27
0.24
0.22
0.22
0.14
0.09
0.09
0.07
0.06
0.05
0.01
44.7)1
160.3
75.8
44.0
7.28
7.94
7.98
10.5
2.20
5.82
4.17
1.22
1.50
2.28
1.86
1.11
0.79
0.07
0.27
0.41
0.23
0.23
0.04
0.05
0.12
0.31
0.2
0.14
0.15
0.08
0.06
0.08
0.01
28.0)3
24.6)2
118.0
2.35)10
0.21)11
7.79
0.67)5
1.93
13.6
1
1.16)8
9.60
3.03
1.06
0
0.66
0.82
2.58
0.29
0.09
0.16
0
0
0.53
0.07
0
0
0.08
0.07
0.01
0.06
0.07
0
4.67)3
6.58)2
107.7
3.32)10
2.51
0.22
0.32)7
1.04
4.28
0.01
0.56)9
2.30
1.33
0.35
0
0.66
2.33
0
0.06
0.03
0.01
0
0
0.85
0
0
0
0.03
0
0.12
0
0
0
1.21
0.26
1.72
0.14
0.03
0
17.15
9.486
0.33
4.01
2.84
0.12
5.52
0.74
0.60
0.81
0.49
0.15
3.81
1.65
1.03
0.77
0.49
0.03
1117
G. J. Edgar et al.
Table 1 continued
Biogeographical region
Species
Far-northern
Northern
South-eastern
Indo-Pacific species
Scarus ghobban Forsskal
Cirrhitichthys oxycephalus (Bleeker)
Acanthurus nigricans Linnaeus
Sphoeroides annulatus (Jenyns)
Zanclus cornutus (Linnaeus)
Scarus rubroviolaceus Bleeker
Aulostomus chinensis Lacepede
Seriola rivoliana Valenciennes
Arothron meleagris (Bloch & Schneider)
Melichthys niger (Bloch)
Elagatis bipinnulata (Quor & Gaimard)
Fistularia commersonii Rüppell
Chilomycterus affinis Günther
Taeniura meyeri (Müller & Henle)
Sphyrna lewini (Griffith & Smith)
Acanthurus xanthopterus Valenciennes
Diodon hystrix Linnaeus
Heteropriacanthus cruentatus (Lacepede)
Triaenodon obesus (Rüppell)
Muraena lentiginosa Jenyns
Diodon holocanthus Linnaeus
Novaculichthys taeniourus (Lacepede)
Aetobatus narinari (Euphrasen)
Myripristis berndti Jordan & Evermann
Ostracion meleagris Shaw
Bothus leopardinus (Günther)
Acanthocybium solandri (Cuvier)
Carcharhinus galapagensis (Snodgrass & Heller)
Arothron hispidus (Linnaeus)
Thalassoma purpureum (Forsskal)
Pseudobalistes naufragium (Jordan & Starks)
0.58
5.616
19.03
0
2.869
1.24
4.797
0.76
1.37
3.08
0.33
0.36
0
0.01
0.79
0.02
0
0.60
0.02
0
0
0.18
0.05
0.02
0
0.04
0
0.05
0
0.06
0
8.12
1.22
0.47
0.01
3.806
0.72
0.42
1.61
1.45
0.26
0.40
0.75
0.01
0.03
0.01
0.01
0.02
0.08
0
0.02
0
0.04
0
0.02
0
0.02
0
0
0.02
0
0
5.20
1.51
0.17
2.47
0.80
0.63
0.08
0.27
0.16
0.17
0.27
0.10
0.14
0.10
0.02
0.10
0.07
0
0.07
0.04
0.06
0.03
0.02
0.02
0.02
0.01
0.02
0.02
0
0
0.01
Widespread species
Paranthias colonus (Günther)
Halichoeres dispilus (Gill)
Ophioblennius steindachneri Jordan & Evermann
Bodianus diplotaenia (Gill)
Holacanthus passer Valenciennes
Abudefduf troschelii (Gill)
Anisotremus interruptus (Gill)
Plagiotremus azaleus (Jordan & Evermann)
Epinephelus labriformis (Jenyns)
Mulloidichthys dentatus (Gill)
Chromis atrilobata Gill
Serranus psittacinus Velenciennes
Trachinotus stilbe (Jordan & Macgregor)
Sufflamen verres (Gilbert & Starks)
Orthopristis chalceus (Günther)
Chaetodon humeralis Günther
Scarus perrico Jordan & Gilbert
Lutjanus argentiventris (Peters)
Nicholsina denticulata (Evermann & Radcliffe)
Kyphosus analogus (Gill)
Apogon pacificus Herre
1033.42
0.90)1
72.84
11.9
7.77)3
0.01
0.1
20.010
1.91
0.5
0.03
0.07
5
4.788
0
0
0.08
0
0
3.3
0
452.6
36.5
33.2
15.9
16.0
2.00)2
15.95
6.96)1
5.42
7.45
3.62
5.573
0.1
2.744
0.05
0.05
0.15
0.1
0.1
0.2
0
604.0
38.4)2
20.7
19.3
16.83
21.64
16.9
9.28
6.31
6.26
6.5
2.61
2.11
1.17
2.28
1.38
1.05
0.69
0.08
0.05
0.21
1118
Western
1.84)7
0.77
0
0.16
0.02
0.02
0
0
0.01
0
0
0.03
0
0.09
0
0.02
0.02
0
0
0.03
0.04
0.02
0.01
0
0
0
0
0
0
0
0.01
234.3)1
90.7
21.0
18.9
7.23)4
0.83
1.30)9
11.9
2.77)6
8.42
4.52
1.4
0
0.09
0.34
0.27
0.58
0.27
1.92
0.01
0
Elizabeth
2.29
0.08
0
0.26
0
0.19
0
0.01
0
0
0
0
0.15
0.03
0
0.02
0.02
0
0
0.09
0.03
0
0
0
0
0
0
0
0
0
0
164.5)1
40.26
4.39)4
21.1)6
2.92)5
3.99)8
0.05
17.81
14.1
0.51
4.96
1.82
0
0.28)11
0.87
0.4
0.05
0.11
0.12
0
0.81
Overall
4.47
1.50
1.49
1.37
1.16
0.55
0.44
0.42
0.39
0.34
0.23
0.19
0.09
0.07
0.07
0.06
0.05
0.05
0.04
0.04
0.04
0.04
0.02
0.02
0.01
0.01
0.01
0.01
0.01
0.01
0.01
511.6
43.6
24.4
18.4
13.2
12.4
11.5
11.0
6.15
5.75
5.19
2.58
1.49
1.39
1.37
0.83
0.68
0.44
0.36
0.29
0.20
Journal of Biogeography 31, 1107–1124, ª 2004 Blackwell Publishing Ltd
Regional biogeography of Galapagos shallow-water reef fauna
Table 1 continued
Biogeographical region
Species
Far-northern
Northern
South-eastern
Western
Elizabeth
Overall
Balistes polylepis Steindachner
Rypticus bicolour Valenciennes
Malacoctenus tetranemus (Cope)
Caulolatilus princeps (Jenyns)
Scomberomorus sierra Jordan & Starks
Alphestes immaculatus Breder
Rypticus nigripinnis Gill
Hippocampus ingens Girard
Stegastes acapulcoensis (Fowler)
0.36
0.05
0.02
0
0.01
0
0
0
0
0.3
0.07
0
0
0
0.04
0.02
0
0.01
0.2
0.25
0.16
0.02
0.13
0.09
0.11
0.02
0.01
0.03
0.06
0.06
0.14
0.02
0.02
0
0.04
0
0
0
0.05
0.65
0.03
0.12
0
0.09
0.06
0.18
0.16
0.10
0.10
0.08
0.07
0.06
0.03
0.01
Table 2 Mean abundance per 100 m2 transect in different biogeographical regions of macro-invertebrate species recorded on at least
two transects. Species identified using SIMPER analysis to be associated with particular bioregions are listed by superscript in rank order
of strength of association, with negative numbers indicating negative association. Taxonomic groups are: E, echinoid; A, asteroid;
H, holothurian; C, crustacean; M, mollusc
Biogeographical region
Species
Taxon
Far-northern
Endemic species
Eucidaris galapagensis (Valenciennes)
Octopus oculifer Hoyle
Scyllarides astori Holthuis
Panamic species
Tripneustes depressus (Agassiz)
Echinometra vanbrunti (Agassiz)
Diadema mexicanum (Agassiz)
Toxopneustes roseus (Agassiz)
Aniculus elegans Stimpson
Holothuria difficilis Semper
Holothuria imitans (Ludwig)
Trizopagurus magnificus (Bouvier)
Holothuria impatiens (Forsckal)
Luidia foliata
E
M
C
54.5)1
0
0
E
E
E
E
C
H
H
C
H
A
0.65)3
0)8
65.41
0.07
0
0
0
0
0.02
0
Indo-Pacific species
Holothuria kefersteini (Selenka)
Holothuria atra (Jaeger)
Stichopus horrens Selenka
Holothuria fuscocinerea (Jaeger)
Mithrodia bradleyi Verrill
Asteropsis carinifera (Lamarck)
Panulirus penicillatus (Olivier)
H
H
H
H
A
A
C
1.22
0.23)7
0.3
0.14
0
0.02
0.55
Widespread species
Lytechinus semituberculatus (Agassiz)
Stichopus fuscus (Ludwig)
Hexaplex princeps (Broderip)
Pentaceraster cumingi (Gray)
Nidorellia armata (Gray)
Centrostephanus coronatus (Verrill)
Phataria unifascialis (Gray)
Pharia pyramidata (Gray)
Linckia columbiae Gray
Percnon gibbesi (H. Milne Edwards)
Pleuroploca princeps Sowerby
E
H
M
A
A
E
A
A
A
C
M
0)2
0.19)4
6.45
0)6
0)5
0)9
0
0
0.02
2.192
0
Northern
South-eastern
Western
Elizabeth
Overall
264.4
0.02
0
392.9
0.07
0.06
252.7
0.22
0.44
280.0
0.18
0
316.8
0.09
0.09
45.2
0.66)6
2.98)3
0.24
0.18
0
0
0.01
0
0
49.11
0.79)4
5.65)3
0.28
0.27
0
0.01
0.01
0
0
29.2
63.24
2.67)3
0
0
0.16
0
0
0
0
2.40)2
230.23
0.70)4
0
0
0.09
0
0
0
0.04
37.6
30.2
8.88
0.19
0.17
0.03
0.01
0.01
0
0
2.95
3.091
0.08
0.802
0.05
0.14
0.01
3.874
2.345
0.72
0.38
0.26
0.07
0.02
0.68)4
0.02)5
0.02
0
0
0
0
2.75
0.03)5
0.03
0
0
0.02
0
2.96
1.75
0.43
0.34
0.15
0.06
0.06
40.7)1
0.96)2
7.82
4.27
0.43)4
1.25)5
0.08)7
0.02
0
0.10
0.02
103.6
1.46)1
9.562
4.833
1.61)2
0.46)5
0.21)6
0.05
0.03
0
0.05
369.31
30.42
5.91)1
1.04)2
11.23
9.355
2.216
0.667
1.41
0.01
0.07
44.3)1
32.51
3.32)3
3.71
11.52
15.35
1.714
1.746
0.40
0
0.10
120.6
8.33
7.96
3.71
3.60
3.18
0.61
0.28
0.26
0.18
0.05
Journal of Biogeography 31, 1107–1124, ª 2004 Blackwell Publishing Ltd
1119
connectivity, and slow recolonization rates when subpopulations have become extinct. A high level of connectivity between
fish populations on different islands is indicated by maximal
fish species richness occurring around the small isolated farnorthern islands of Darwin and Wolf. The only explanation for
this observation within the framework of current island
biogeography theory is that high immigration rates prevail
(Whittaker, 1998). By contrast, macro-invertebrate species
richness was lowest amongst the isolated far-northern islands,
a clear indication that immigration rates are less than for
fishes.
Implications for conservation management
Governments worldwide are increasingly recognizing that
conservation of marine biodiversity requires inter alia a
network of wildlife refuges such as marine protected areas
(MPAs) that are distributed across all biogeographical regions
within their jurisdiction (Australian and New Zealand Environment and Conservation Council Task Force on Marine
Protected Areas, 1999; Roff & Taylor, 2000; Roff & Evans,
2002). In most cases, the biogeographical framework for
reserves is defined using geophysical approaches, with regions
classified in terms of abiotic factors such as salinity,
temperature, depth, rock type or sediment particle size that
are considered surrogates for biota (Roff et al., 2003). However, physical factors rarely act in synchrony, and congruence
between physical and biological regionalizations has rarely
been assessed.
Biological as well as physical regionalizations can vary
greatly, depending on which component of the biota is
analysed. For example, a Tasmanian bioregionalization based
on shallow reef biota exhibited few similarities to one based
on the estuarine fauna (Edgar et al., 1997, 2000). Clearly,
regionalizations used for marine management should reflect
the management target, either directly or by using physical
surrogates shown to covary closely with the subject of
primary interest. In the case of MPA networks, areas are
designated primarily to protect fished species and associated
ecosystems. For this reason, our Galapagos marine bioregionalization was based on inshore reef ecosystems, the habitat
most heavily targeted by local fishers. Sea cucumbers and
0.2
0.1
0
– 0.1
– 0.2
CAP 3
0.1
0
– 0.1
– 0.2
– 0.1
0
0.1
0.2
CAP 1
Table 4 Classification of invertebrate data
pertaining to 0.01 · 0.01 grid cells to five
biogeographical regions using the leaveone-out procedure of canonical analysis of
principal coordinates
Region
Far-northern Northern South-eastern Western Elizabeth Total Correct (%)
Far-northern
Northern
South-eastern
Western
Elizabeth
5
0
1
0
0
lobsters captured by divers provided > 80% of the total
annual income of fishers over the past 5 years (Murillo,
2002).
1
15
28
0
0
0
8
77
1
0
0
0
4
26
3
0
0
2
9
11
6
23
112
36
14
0.83
0.65
0.69
0.72
0.79
Conservation of marine biodiversity in Galapagos would be
assisted by a change in the GMR Management Plan from
recognition of the Harris biogeographical regions to the five
G. J. Edgar et al.
Table 5 Area (km2) included in different management zones
for the five biogeographical regions defined in this study
(Valle, 1995), Galapagos penguin (Boersma, 1998) and
Galapagos fur seal (Trillmich & Limberger, 1985).
Management zone, km2 (%)
Biogeographical
Conservation Tourism
Fishing
region
ACKNOWLEDGMENTS
Far-northern
Northern
South-eastern
Western
Elizabeth
Total
0.78
6.23
68.88
36.61
7.68
120.17
(4.6)
(5.5)
(7.7)
(11.2)
(4.8)
3.78
18.25
98.92
26.37
16.80
164.12
(22.2)
(16.0)
(11.0)
(8.1)
(10.6)
12.46
89.46
731.49
262.93
134.64
1230.98
Total
(73.2)
(78.5)
(81.3)
(80.7)
(84.6)
17.02
113.94
899.29
325.91
159.12
1515.27
biogeographical regions outlined here. During consensual
discussions in 2000, stakeholders of the GMR agreed on
preliminary ‘no-take’ conservation zones to protect coastal
ecosystems within each of the five Harris zones; however,
disproportionately low levels of protection have consequently
been afforded to the small distinctive ecosystems in the farnorthern and Elizabeth bioregions.
The far-northern region has very high conservation significance due to its distinctive biota with anomalously high
species richness of fishes and corals. The area reserved for
conservation purposes within this bioregion is very small
(0.78 km2, Table 5), in part because the bioregion itself is so
small, comprising two islands only.
The Elizabeth bioregion includes the smallest percentage of
coast zoned for conservation amongst the five Galapagos
biogeographical regions described here (Table 5), with only a
single small area around Islas Marielas fully protected. A
notable feature of this bioregion is a disproportionately high
number of endemic Galapagos species, making it the core area
for much of the endemic Galapagos inshore marine fauna and
possibly an important refuge for local Galapagos species during
periods of adverse environmental conditions such as El Niño.
Thus, despite its low overall species richness, the Elizabeth
bioregion should be considered an area with exceptional
conservation significance.
The inverse relationship evident at regional scales in
Galapagos between the richness of the total fish fauna and
the richness of endemic fish species has broad management
implications. In the terrestrial environment, several authors
have suggested that conservation areas should be prioritized
spatially in terms of ‘hotspots’ of biodiversity (Meyers et al.,
2000). Roberts et al. (2002) extended this concept to the
marine realm, arguing that centres of marine endemism in the
Pacific are congruent with hotspots of species richness (but for
alternate view see Hughes et al., 2002). A hotspot strategy for
Galapagos, in the absence of gap analysis, would indicate a low
conservation rating for western Galapagos and Elizabeth
ecosystems, whereas on a global scale these areas possess
highest conservation significance. The western upwelling
region provides core habitat for virtually all endemic Galapagos marine taxa, including many charismatic species not
included in the present study, such as the flightless cormorant
1122
We would like to thank the various divers who assisted us
collecting data, particularly Lauren Garske, Noemi D’Ozouville, Linda Kerrison, Fernando Rivera, Vicente Almardariz,
Veronica Toral-Granda, Scoresby Shepherd, Giancarlo Toti,
Julio Delgado, Angel Chiriboga, Diego Ruiz and Vanessa
Francesco. Support for the monitoring program provided by
Galapagos National Park Service, and funding by USAID, the
Charles Darwin Foundation Inc., Galapagos Conservation
Trust, the British Embassy, Beneficia Foundation, Pew Charitable Trust and Rockefeller Foundation is gratefully acknowledged. We also thank Rodrigo Bustamante and Robert
Bensted-Smith for organizing funding proposals, and Marti
Anderson for statistical advice on using the CAP program.
REFERENCES
Anderson, M.J. (2003) CAP: a FORTRAN computer program
for canonical analysis of principal coordinates. Department of
Statistics, University of Auckland, Auckland, New Zealand.
Anderson, M.J. & Robinson, J. (2003) Generalised discriminant analysis based on distances. Australian and New
Zealand Journal of Statistics, 45, 301–318.
Anderson, M.J. & Willis, T.J. (2003) Canonical analysis of
principal coordinates: a useful method of constrained ordination for ecology. Ecology, 84, 511–524.
Australian and New Zealand Environment and Conservation
Council Task Force on Marine Protected Areas (1999)
Strategic plan of action for the National Representative System
of Marine Protected Areas: a guide for action by Australian
Governments. Environment Australia, Canberra.
Banks, S.J. (2002) Ambiente Fı́sico. Reserva Marina de Galápagos, Lı́nea Base de la Biodiversidad (ed. by E. Danulat and
G.J. Edgar), pp. 18–33. Charles Darwin Foundation and
Galápagos National Park Service, Galápagos, Ecuador.
Bensted-Smith, R. (2002) A biodiversity vision for the Galapagos
Islands. Charles Darwin Foundation and World Wildlife
Fund, Puerto Ayora, Galapagos, Ecuador.
Boersma, P.D. (1998) Population trends of the Galapagos
penguin: impacts of El Nino and La Nina. Condor, 100, 245–
253.
Bustamante, R., Collins, K.J. & Bensted-Smith, R. (2000)
Biodiversity conservation in the Galápagos Marine Reserve.
Bulletin de l’Institut Royal des Sciences Naturelles de Belgigue,
Supplement 70, 31–38.
Bustamante, R.H., Vinueza, L.R., Smith, F., Banks, S., Calvopiña, M., Francisco, V., Chiriboga, A. & Harris, J. (2002)
Comunidades submareales rocosas. I: Organismos sésiles y
mesoinvertebrados móviles. Reserva Marina de Galápagos,
Lı́nea Base de la Biodiversidad (eds E. Danulat and G.J.
Edgar), pp. 33–62. Charles Darwin Foundation and
Galápagos National Park Service, Galápagos, Ecuador.
Journal of Biogeography 31, 1107–1124, ª 2004 Blackwell Publishing Ltd
Cairns, S.D. (1991) A revision of the ahermatypic Scleractinia
of the Galápagos and Cocos Islands. Smithsonian Contributions in Zoology, 504, 1–32.
Carr, M.R. (1996) PRIMER User Manual. Plymouth Routines in
Multivariate Ecological Research. Plymouth Marine Laboratory, Plymouth, UK.
Clarke, K.R. (1993) Non-parametric multivariate analyses of
changes in community structure. Australian Journal of
Ecology,18, 117–143.
Edgar, G.J., Moverley, J., Barrett, N.S., Peters, D. & Reed, C.
(1997) The conservation-related benefits of a systematic
marine biological sampling program: the Tasmanian reef
bioregionalisation as a case study. Biological Conservation,
79, 227–240.
Edgar, G.J., Barrett, N.S., Graddon, D.J. & Last, P.R. (2000)
The conservation significance of estuaries: a classification
of Tasmanian estuaries using ecological, physical and
demographic attributes as a case study. Biological Conservation, 92, 383–397.
Faith, D.P., Minchin, P.R. & Belbin, L. (1987) Compositional
dissimilarity as a robust measure of ecological distance.
Vegetatio, 69, 57–68.
Glynn, P.W. (1994) State of coral reefs in the Galapagos Islands: natural vs anthropogenic impacts. Marine Pollution
Bulletin, 29, 131–140.
Glynn, P.W. & Ault, J.S. (2000) A biogeographic analysis and
review of the far eastern Pacific coral reef region. Coral Reefs,
19, 1–23.
Grove, J.S. (1985) Influence of the 1982–1983 El Niño event
upon the ichthyofauna of the Galápagos archipelago. El Niño
in the Galápagos Islands: the 1982–1983 Event (ed. by G.
Robinson and E.M. Del Pino), pp. 191–198. Charles Darwin
Foundation
,
for17a603 p), G(th3513.3603 0.0506 TD(´)Tj0.3541 -0.0506 TD[(92(of)-480.9[(G0.1(aQuito[(G0uponEcuadory)-472(G0o)Tjj-6.2091 -
G. J. Edgar et al.
BIOSKETCHES
Graham Edgar recently returned to Tasmania after 2 years as Head of Marine Science at the Charles Darwin Research Station,
Galapagos. He has investigated a variety of ecological interactions in the marine environment, primarily those involving human
impacts.
Stuart Banks is mainly interests in physical oceanography, particularly the interpretation of oceanographical patterns at large
spatial scales using satellite imagery.
José Miguel Fariña currently holds a faculty position at the Center for Advanced Studies in Ecology and Biodiversity, Santiago,
after returning from postdoctoral studies at Brown University. His research has focussed on ecotrophic transfer between land and sea
and impacts of human activity on fishes and benthos.
Mónica Calvopiña is primarily interested in community ecology and the social implications of marine research, particularly as they
affect inhabitants of her Galapagos birthplace.
Camilo Martı́nez recently completed a masters degree in marine resource management in the Canary Islands. He has worked
extensively on the biology of fishery species, most notably the Galapagos spiny lobster.
1124
Journal of Biogeography 31, 1107–1124, ª 2004 Blackwell Publishing Ltd